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Cited by 138Neural dynamics and brain functionMotor Control and AdaptationMemory and Neural Mechanisms

Spatial gradients and multidimensional dynamics in a neural integrator circuit

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Miri, Andrew, Daie, Kayvon, Arrenberg, Aristides B, Baier, Herwig, Aksay, Emre, Tank, David W·2011·Nature Neuroscience
DOI 10.1038/nn.2888PMC PMC3624014
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Abstract

In a neural integrator, the variability and topographical organization of neuronal firing-rate persistence can provide information about the circuit's functional architecture. We used optical recording to measure the time constant of decay of persistent firing (persistence time) across a population of neurons comprising the larval zebrafish oculomotor velocity-to-position neural integrator. We found extensive persistence time variation (tenfold; coefficients of variation = 0.58-1.20) across cells in individual larvae. We also found that the similarity in firing between two neurons decreased as the distance between them increased and that a gradient in persistence time was mapped along the rostrocaudal and dorsoventral axes. This topography is consistent with the emergence of persistence time heterogeneity from a circuit architecture in which nearby neurons are more strongly interconnected than distant ones. Integrator circuit models characterized by multiple dimensions of slow firing-rate dynamics can account for our results.

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  • The connectome for the VPNI contains two weakly coupled three-block cycles that lead to a corresponding pair of large real eigenvalues, providing an anatomical basis for the low-dimensional neural activity observed in this network.

    “we found the connectome for the VPNI to contain two weakly coupled three-block cycles that lead to a corresponding pair of large real eigenvalues, providing an anatomical basis for the low-dimensional neural activity observed in this network16,55.”

    From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [55]

    The Results (Distributed firing rate persistence times) report multiple distinct persistence times, and the Discussion says the observed hVPNI firing dynamics are multidimensional. That supports the citation’s reference to organized neural dynamics, but our copy does not establish that the activity is specifically low-dimensional. The connectome cycles and eigenvalues are presented as the citing authors’ own finding, not as a finding attributed to this source. (LLM, conf=0.79)

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  • This extension is consistent with a previous observation that VPNI function was only partially abolished by sizable inactivation of R7/R8 and with previous reports of eye position signals in R4-R6 neurons that are not from ABD neurons.

    “This extension is consistent with a previous observation that VPNI function was only partially abolished by sizable inactivation of R7/R8 (ref. 55) and with previous reports of eye position signals in R4–R6 neurons that are not from ABD neurons50,57.”

    From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [55]

  • This cyclic structure may be required for control of the eye plant, which can be approximated as a highly damped mass-spring system whose impulse-response function exhibits overdamped oscillations, and may suggest the importance of a weak, but non-negligible, mass term in the plant.

    “This may be required for control of the eye plant, which can be approximated as a highly damped mass-spring system whose impulse-response function exhibits overdamped oscillations59 and may suggest the importance of a weak, but non-negligible, mass term in the plant that is commonly ignored in simplified descriptions55,60.”

    From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [55]

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References 52 · Cited by 138

Research works printed but not linked: 41

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Authors
Miri, A., Daie, K., Arrenberg, A. B., Baier, H., Aksay, E., & Tank, D. W.
Affiliations
  • Princeton University (US)
  • Cornell University (US)
  • University of Freiburg (DE)
Corresponding author
  • Aksay, Emre
  • Tank, David W
ORCID
Venue
Nature Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2011-08-21
Volume
14
Issue
9
Pages
1150-1159
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
DOI
10.1038/nn.2888
PMC
PMC3624014
OpenAlex
W2068717605
Cited by
138
References
52
Citations by year
2026: 3 · 2025: 6 · 2024: 5 · 2023: 7 · 2022: 12 · 2021: 9 · 2020: 7 · 2019: 16 · 2018: 7 · 2017: 10 · 2016: 12 · 2015: 10 · 2014: 17 · 2013: 10 · 2012: 7
FWCI
5.52
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Princeton University
  • National Institute of Mental Health (R01MH060651)
  • National Eye Institute (T32EY007138)
  • National Institute of Neurological Disorders and Stroke (R01NS053358)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
neural integrator, persistent firing, persistence time, oculomotor system, zebrafish larvae, topographic organization, neuronal connectivity, firing rate dynamics, circuit architecture, spatial gradients, rostrocaudal axis, dorsal-ventral axis
MeSH terms
Action Potentials, Animals, Brain Stem, Calcium, Computer Simulation, Eye Movements, Gene Expression Regulation, Larva, Functional Laterality, Light, Models, Neurological, Nerve Net, Neurons, Photic Stimulation, Time Factors, Zebrafish, Nonlinear Dynamics, Zebrafish Proteins, Animals, Genetically Modified, Microphthalmia-Associated Transcription Factor

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